Chimeric symbionts expressing a Wolbachia protein stimulate mosquito immunity and inhibit filarial parasite development

Sara Epis; Ilaria Varotto-Boccazzi; Elena Crotti; Claudia Damiani; Laura Giovati; Mauro Mandrioli; Marco Biggiogera; Paolo Gabrieli; Marco Genchi; Luciano Polonelli; Daniele Daffonchio; Guido Favia; Claudio Bandi

doi:10.1038/s42003-020-0835-2

Chimeric symbionts expressing a Wolbachia protein stimulate mosquito immunity and inhibit filarial parasite development

Sara Epis, Ilaria Varotto-Boccazzi, Elena Crotti, Claudia Damiani, Laura Giovati, Mauro Mandrioli, Marco Biggiogera, Paolo Gabrieli, Marco Genchi, Luciano Polonelli, Daniele Daffonchio, Guido Favia, Claudio Bandi

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19 Scopus citations

Abstract

Wolbachia can reduce the capability of mosquitoes to transmit infectious diseases to humans and is currently exploited in campaigns for the control of arboviruses, like dengue and Zika. Under the assumption that Wolbachia-mediated activation of insect immunity plays a role in the reduction of mosquito vectorial capacity, we focused our attention on the Wolbachia surface protein (WSP), a potential inductor of innate immunity. We hypothesized that the heterologous expression of this protein in gut- and tissue-associated symbionts may reduce parasite transmission. We thus engineered the mosquito bacterial symbiont Asaia to express WSP (AsaiaWSP). AsaiaWSP induced activation of the host immune response in Aedes aegypti and Anopheles stephensi mosquitoes, and inhibited the development of the heartworm parasite Dirofilaria immitis in Ae. aegypti. These results consolidate previous evidence on the immune-stimulating property of WSP and make AsaiaWSP worth of further investigations as a potential tool for the control of mosquito-borne diseases.

Original language	English (US)
Journal	Communications Biology
Volume	3
Issue number	1
DOIs	https://doi.org/10.1038/s42003-020-0835-2
State	Published - Mar 6 2020

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: This study was supported by Cariplo Foundation and Lombardy Region to S.E. (2017-N.1656), by Transition Grant 2015-2017-Horizon 2020 to S.E. (G42F17000140001) and by the MIUR PRIN (Italian Ministry of Education, University and Research, MIUR) to C.B., L.P. and G.F. D.D. acknowledges the baseline funding support by King Abdullah University of Science and Technology (KAUST); S.E., C.B. and M.B. thank “Fondo per il finanziamento dei Dipartimenti universitari di eccellenza” (MIUR) of the Dept. of Biosciences (University of Milan) and of the Dept. of Biology and Biotechnology “L. Spallanzani” (University of Pavia). The authors thank Prof. L. Sacchi, Prof. F. Forlani and Prof. C. Bazzocchi for their suggestions and the UNITECH platform for the microscope image acquisition.

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10.1038/s42003-020-0835-2

https://repository.kaust.edu.sa/bitstream/10754/661952/1/s42003-020-0835-2.pdf

Cite this

Epis, S., Varotto-Boccazzi, I., Crotti, E., Damiani, C., Giovati, L., Mandrioli, M., Biggiogera, M., Gabrieli, P., Genchi, M., Polonelli, L., Daffonchio, D., Favia, G., & Bandi, C. (2020). Chimeric symbionts expressing a Wolbachia protein stimulate mosquito immunity and inhibit filarial parasite development. Communications Biology, 3(1). https://doi.org/10.1038/s42003-020-0835-2

@article{61edc6018bec4de0a2bd3de76f5903a8,

title = "Chimeric symbionts expressing a Wolbachia protein stimulate mosquito immunity and inhibit filarial parasite development",

abstract = "Wolbachia can reduce the capability of mosquitoes to transmit infectious diseases to humans and is currently exploited in campaigns for the control of arboviruses, like dengue and Zika. Under the assumption that Wolbachia-mediated activation of insect immunity plays a role in the reduction of mosquito vectorial capacity, we focused our attention on the Wolbachia surface protein (WSP), a potential inductor of innate immunity. We hypothesized that the heterologous expression of this protein in gut- and tissue-associated symbionts may reduce parasite transmission. We thus engineered the mosquito bacterial symbiont Asaia to express WSP (AsaiaWSP). AsaiaWSP induced activation of the host immune response in Aedes aegypti and Anopheles stephensi mosquitoes, and inhibited the development of the heartworm parasite Dirofilaria immitis in Ae. aegypti. These results consolidate previous evidence on the immune-stimulating property of WSP and make AsaiaWSP worth of further investigations as a potential tool for the control of mosquito-borne diseases.",

author = "Sara Epis and Ilaria Varotto-Boccazzi and Elena Crotti and Claudia Damiani and Laura Giovati and Mauro Mandrioli and Marco Biggiogera and Paolo Gabrieli and Marco Genchi and Luciano Polonelli and Daniele Daffonchio and Guido Favia and Claudio Bandi",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: This study was supported by Cariplo Foundation and Lombardy Region to S.E. (2017-N.1656), by Transition Grant 2015-2017-Horizon 2020 to S.E. (G42F17000140001) and by the MIUR PRIN (Italian Ministry of Education, University and Research, MIUR) to C.B., L.P. and G.F. D.D. acknowledges the baseline funding support by King Abdullah University of Science and Technology (KAUST); S.E., C.B. and M.B. thank “Fondo per il finanziamento dei Dipartimenti universitari di eccellenza” (MIUR) of the Dept. of Biosciences (University of Milan) and of the Dept. of Biology and Biotechnology “L. Spallanzani” (University of Pavia). The authors thank Prof. L. Sacchi, Prof. F. Forlani and Prof. C. Bazzocchi for their suggestions and the UNITECH platform for the microscope image acquisition.",

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Epis, S, Varotto-Boccazzi, I, Crotti, E, Damiani, C, Giovati, L, Mandrioli, M, Biggiogera, M, Gabrieli, P, Genchi, M, Polonelli, L, Daffonchio, D, Favia, G & Bandi, C 2020, 'Chimeric symbionts expressing a Wolbachia protein stimulate mosquito immunity and inhibit filarial parasite development', Communications Biology, vol. 3, no. 1. https://doi.org/10.1038/s42003-020-0835-2

TY - JOUR

T1 - Chimeric symbionts expressing a Wolbachia protein stimulate mosquito immunity and inhibit filarial parasite development

AU - Epis, Sara

AU - Varotto-Boccazzi, Ilaria

AU - Crotti, Elena

AU - Damiani, Claudia

AU - Giovati, Laura

AU - Mandrioli, Mauro

AU - Biggiogera, Marco

AU - Gabrieli, Paolo

AU - Genchi, Marco

AU - Polonelli, Luciano

AU - Daffonchio, Daniele

AU - Favia, Guido

AU - Bandi, Claudio

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: This study was supported by Cariplo Foundation and Lombardy Region to S.E. (2017-N.1656), by Transition Grant 2015-2017-Horizon 2020 to S.E. (G42F17000140001) and by the MIUR PRIN (Italian Ministry of Education, University and Research, MIUR) to C.B., L.P. and G.F. D.D. acknowledges the baseline funding support by King Abdullah University of Science and Technology (KAUST); S.E., C.B. and M.B. thank “Fondo per il finanziamento dei Dipartimenti universitari di eccellenza” (MIUR) of the Dept. of Biosciences (University of Milan) and of the Dept. of Biology and Biotechnology “L. Spallanzani” (University of Pavia). The authors thank Prof. L. Sacchi, Prof. F. Forlani and Prof. C. Bazzocchi for their suggestions and the UNITECH platform for the microscope image acquisition.

PY - 2020/3/6

Y1 - 2020/3/6

N2 - Wolbachia can reduce the capability of mosquitoes to transmit infectious diseases to humans and is currently exploited in campaigns for the control of arboviruses, like dengue and Zika. Under the assumption that Wolbachia-mediated activation of insect immunity plays a role in the reduction of mosquito vectorial capacity, we focused our attention on the Wolbachia surface protein (WSP), a potential inductor of innate immunity. We hypothesized that the heterologous expression of this protein in gut- and tissue-associated symbionts may reduce parasite transmission. We thus engineered the mosquito bacterial symbiont Asaia to express WSP (AsaiaWSP). AsaiaWSP induced activation of the host immune response in Aedes aegypti and Anopheles stephensi mosquitoes, and inhibited the development of the heartworm parasite Dirofilaria immitis in Ae. aegypti. These results consolidate previous evidence on the immune-stimulating property of WSP and make AsaiaWSP worth of further investigations as a potential tool for the control of mosquito-borne diseases.

AB - Wolbachia can reduce the capability of mosquitoes to transmit infectious diseases to humans and is currently exploited in campaigns for the control of arboviruses, like dengue and Zika. Under the assumption that Wolbachia-mediated activation of insect immunity plays a role in the reduction of mosquito vectorial capacity, we focused our attention on the Wolbachia surface protein (WSP), a potential inductor of innate immunity. We hypothesized that the heterologous expression of this protein in gut- and tissue-associated symbionts may reduce parasite transmission. We thus engineered the mosquito bacterial symbiont Asaia to express WSP (AsaiaWSP). AsaiaWSP induced activation of the host immune response in Aedes aegypti and Anopheles stephensi mosquitoes, and inhibited the development of the heartworm parasite Dirofilaria immitis in Ae. aegypti. These results consolidate previous evidence on the immune-stimulating property of WSP and make AsaiaWSP worth of further investigations as a potential tool for the control of mosquito-borne diseases.

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DO - 10.1038/s42003-020-0835-2

M3 - Article

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SN - 2399-3642

VL - 3

JO - Communications Biology

JF - Communications Biology

IS - 1

ER -

Chimeric symbionts expressing a Wolbachia protein stimulate mosquito immunity and inhibit filarial parasite development

Abstract

Bibliographical note

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